Introducing the Microbes and Social Equity Working Group: Considering the Microbial Components of Social, Environmental, and Health Justice.

Humans are inextricably linked to each other and our natural world, and microorganisms lie at the nexus of those interactions. Microorganisms form genetically flexible, taxonomically diverse, and biochemically rich communities, i.e., microbiomes that are integral to the health and development of macroorganisms, societies, and ecosystems. Yet engagement with beneficial microbiomes is dictated by access to public resources, such as nutritious food, clean water and air, safe shelter, social interactions, and effective medicine. In this way, microbiomes have sociopolitical contexts that must be considered. The Microbes and Social Equity (MSE) Working Group connects microbiology with social equity research, education, policy, and practice to understand the interplay of microorganisms, individuals, societies, and ecosystems. Here, we outline opportunities for integrating microbiology and social equity work through broadening education and training; diversifying research topics, methods, and perspectives; and advocating for evidence-based public policy that supports sustainable, equitable, and microbial wealth for all.

Viable bacterial communities on hospital window components in patient rooms.

Previous studies demonstrate an exchange of bacteria between hospital room surfaces and patients, and a reduction in survival of microorganisms in dust inside buildings from sunlight exposure. While the transmission of microorganisms between humans and their local environment is a continuous exchange which generally does not raise cause for alarm, in a hospital setting with immunocompromised patients, these building-source microbial reservoirs may pose a risk. Window glass is often neglected during hospital disinfection protocols, and the microbial communities found there have not previously been examined. This pilot study examined whether living bacterial communities, and specifically the pathogens Methicillin-resistant Staphylococcus aureus (MRSA) and Clostridioides difficile (C. difficile), were present on window components of exterior-facing windows inside patient rooms, and whether relative light exposure (direct or indirect) was associated with changes in bacterial communities on those hospital surfaces. Environmental samples were collected from 30 patient rooms in a single ward at Oregon Health & Science University (OHSU) in Portland, Oregon, USA. Sampling locations within each room included the window glass surface, both sides of the window curtain, two surfaces of the window frame, and the air return grille. Viable bacterial abundances were quantified using qPCR, and community composition was assessed using Illumina MiSeq sequencing of the 16S rRNA gene V3/V4 region. Viable bacteria occupied all sampled locations, but was not associated with a specific hospital surface or relative sunlight exposure. Bacterial communities were similar between window glass and the rest of the room, but had significantly lower Shannon Diversity, theorized to be related to low nutrient density and resistance to bacterial attachment of glass compared to other surface materials. Rooms with windows that were facing west demonstrated a higher abundance of viable bacteria than those facing other directions, potentially because at the time of sampling (morning) west-facing rooms had not yet been exposed to sunlight that day. Viable C. difficile was not detected and viable MRSA was detected at very low abundance. Bacterial abundance was negatively correlated with distance from the central staff area containing the break room and nursing station. In the present study, it can be assumed that there is more human traffic in the center of the ward, and is likely responsible for the observed gradient of total abundance in rooms along the ward, as healthcare staff both deposit more bacteria during activities and affect microbial transit indoors. Overall, hospital window components possess similar microbial communities to other previously identified room locations known to act as reservoirs for microbial agents of hospital-associated infections.

Accumulation of di-2-ethylhexyl phthalate from polyvinyl chloride flooring into settled house dust and the effect on the bacterial community.

Di-2-ethylhexyl phthalate (DEHP) is a plasticizer used in consumer products and building materials, including polyvinyl chloride flooring material. DEHP adsorbs from material and leaches into soil, water, or dust and presents an exposure risk to building occupants by inhalation, ingestion, or absorption. A number of bacterial isolates are demonstrated to degrade DEHP in culture, but bacteria may be susceptible to it as well, thus this study examined the relation of DEHP to bacterial communities in dust. Polyvinyl chloride flooring was seeded with homogenized house dust and incubated for up to 14 days, and bacterial communities in dust were identified at days 1, 7, and 14 using the V3-V4 regions of the bacterial 16S rRNA gene. DEHP concentration in dust increased over time, as expected, and bacterial richness and Shannon diversity were negatively correlated with DEHP concentration. Some sequence variants of Bacillus, Corynebacterium jeddahense, Streptococcus, and Peptoniphilus were relatively more abundant at low concentrations of DEHP, while some Sphingomonas, Chryseobacterium, and a member of the Enterobacteriaceae family were relatively more abundant at higher concentrations. The built environment is known to host lower microbial diversity and biomass than natural environments, and DEHP or other chemicals indoors may contribute to this paucity.

Antimicrobial Chemicals Associate with Microbial Function and Antibiotic Resistance Indoors.

Humans purposefully and inadvertently introduce antimicrobial chemicals into buildings, resulting in widespread compounds, including triclosan, triclocarban, and parabens, in indoor dust. Meanwhile, drug-resistant infections continue to increase, raising concerns that buildings function as reservoirs of, or even select for, resistant microorganisms. Support for these hypotheses is limited largely since data describing relationships between antimicrobials and indoor microbial communities are scant. We combined liquid chromatography-isotope dilution tandem mass spectrometry with metagenomic shotgun sequencing of dust collected from athletic facilities to characterize relationships between indoor antimicrobial chemicals and microbial communities. Elevated levels of triclosan and triclocarban, but not parabens, were associated with distinct indoor microbiomes. Dust of high triclosan content contained increased Gram-positive species with diverse drug resistance capabilities, whose pangenomes were enriched for genes encoding osmotic stress responses, efflux pump regulation, lipid metabolism, and material transport across cell membranes; such triclosan-associated functional shifts have been documented in laboratory cultures but not yet from buildings. Antibiotic-resistant bacterial isolates were cultured from all but one facility, and resistance often increased in buildings with very high triclosan levels, suggesting links between human encounters with viable drug-resistant bacteria and local biocide conditions. This characterization uncovers complex relationships between antimicrobials and indoor microbiomes: some chemicals elicit effects, whereas others may not, and no single functional or resistance factor explained chemical-microbe associations. These results suggest that anthropogenic chemicals impact microbial systems in or around buildings and their occupants, highlighting an emergent need to identify the most important indoor, outdoor, and host-associated sources of antimicrobial chemical-resistome interactions. IMPORTANCE The ubiquitous use of antimicrobial chemicals may have undesired consequences, particularly on microbes in buildings. This study shows that the taxonomy and function of microbes in indoor dust are strongly associated with antimicrobial chemicals-more so than any other feature of the buildings. Moreover, we identified links between antimicrobial chemical concentrations in dust and culturable bacteria that are cross-resistant to three clinically relevant antibiotics. These findings suggest that humans may be influencing the microbial species and genes that are found indoors through the addition and removal of particular antimicrobial chemicals.

Daylight exposure modulates bacterial communities associated with household dust.

BACKGROUND: Microbial communities associated with indoor dust abound in the built environment. The transmission of sunlight through windows is a key building design consideration, but the effects of light exposure on dust communities remain unclear. We report results of an experiment and computational models designed to assess the effects of light exposure and wavelengths on the structure of the dust microbiome. Specifically, we placed household dust in replicate model "rooms" with windows that transmitted visible, ultraviolet, or no light and measured taxonomic compositions, absolute abundances, and viabilities of the resulting bacterial communities. RESULTS: Light exposure per se led to lower abundances of viable bacteria and communities that were compositionally distinct from dark rooms, suggesting preferential inactivation of some microbes over others under daylighting conditions. Differences between communities experiencing visible and ultraviolet light wavelengths were relatively minor, manifesting primarily in abundances of dead human-derived taxa. Daylighting was associated with the loss of a few numerically dominant groups of related microorganisms and apparent increases in the abundances of some rare groups, suggesting that a small number of microorganisms may have exhibited modest population growth under lighting conditions. Although biological processes like population growth on dust could have generated these patterns, we also present an alternate statistical explanation using sampling models from ecology; simulations indicate that artefactual, apparent increases in the abundances of very rare taxa may be a null expectation following the selective inactivation of dominant microorganisms in a community. CONCLUSIONS: Our experimental and simulation-based results indicate that dust contains living bacterial taxa that can be inactivated following changes in local abiotic conditions and suggest that the bactericidal potential of ordinary window-filtered sunlight may be similar to ultraviolet wavelengths across dosages that are relevant to real buildings.

Assessment of human exposure to triclocarban, triclosan and five parabens in U.S. indoor dust using dispersive solid phase extraction followed by liquid chromatography tandem mass spectrometry.

Antimicrobials in indoor dust pose concerns due to their endocrine disrupting activities and potential promotion of antibiotic resistance. We adopted dispersive solid phase extraction (d-SPE) and liquid chromatography-tandem mass spectrometry (LC-MS/MS) to quantify antimicrobials in dust. The method showed favorable linearity (R2 >0.99), recovery (83-115%), and method detection limits (1.2-5.6 ng/g, dry weight). All seven analytes were found at median concentrations in ng/g in each of the 80 U.S. dust samples collected from athletic facilities and residential homes: methyl paraben (1920) > propyl paraben (965) > triclosan (390) > triclocarban (270) > ethyl paraben (195) > butyl paraben (80) > benzyl paraben (6). Triclosan levels in dust from athletic facilities were significantly higher than those in private homes (p < 0.05). Median estimated daily intake (EDI) of antimicrobials in ng/kg-body weight/d from dust ingestion was lowest for adults (1.9) and higher for more sensitive subpopulations, including infants (19.8), toddlers (23.6), children (11.8) and teenagers (4.6). This first application of d-SPE to the analysis of dust produced U.S. baseline data for triclosan and triclocarban levels in indoor dust just prior to the 2017 Federal ban on use of these trichlorinated aromatics in antiseptic soaps and related personal care products.

Antimicrobial Chemicals Are Associated with Elevated Antibiotic Resistance Genes in the Indoor Dust Microbiome.

Antibiotic resistance is increasingly widespread, largely due to human influence. Here, we explore the relationship between antibiotic resistance genes and the antimicrobial chemicals triclosan, triclocarban, and methyl-, ethyl-, propyl-, and butylparaben in the dust microbiome. Dust samples from a mixed-use athletic and educational facility were subjected to microbial and chemical analyses using a combination of 16S rRNA amplicon sequencing, shotgun metagenome sequencing, and liquid chromatography tandem mass spectrometry. The dust resistome was characterized by identifying antibiotic resistance genes annotated in the Comprehensive Antibiotic Resistance Database (CARD) from the metagenomes of each sample using the Short, Better Representative Extract Data set (ShortBRED). The three most highly abundant antibiotic resistance genes were tet(W), blaSRT-1, and erm(B). The complete dust resistome was then compared against the measured concentrations of antimicrobial chemicals, which for triclosan ranged from 0.5 to 1970 ng/g dust. We observed six significant positive associations between the concentration of an antimicrobial chemical and the relative abundance of an antibiotic resistance gene, including one between the ubiquitous antimicrobial triclosan and erm(X), a 23S rRNA methyltransferase implicated in resistance to several antibiotics. This study is the first to look for an association between antibiotic resistance genes and antimicrobial chemicals in dust.

Making microbiology of the built environment relevant to design.

Architects are enthusiastic about "bioinformed design" as occupant well-being is a primary measure of architectural success. However, architects are also under mounting pressure to create more sustainable buildings. Scientists have a critical opportunity to make the emerging field of microbiology of the built environment more relevant and applicable to real-world design problems by addressing health and sustainability in tandem. Practice-based research, which complements evidence-based design, represents a promising approach to advancing knowledge of the indoor microbiome and translating it to architectural practice.

Architectural design drives the biogeography of indoor bacterial communities.

BACKGROUND: Architectural design has the potential to influence the microbiology of the built environment, with implications for human health and well-being, but the impact of design on the microbial biogeography of buildings remains poorly understood. In this study we combined microbiological data with information on the function, form, and organization of spaces from a classroom and office building to understand how design choices influence the biogeography of the built environment microbiome. RESULTS: Sequencing of the bacterial 16S gene from dust samples revealed that indoor bacterial communities were extremely diverse, containing more than 32,750 OTUs (operational taxonomic units, 97% sequence similarity cutoff), but most communities were dominated by Proteobacteria, Firmicutes, and Deinococci. Architectural design characteristics related to space type, building arrangement, human use and movement, and ventilation source had a large influence on the structure of bacterial communities. Restrooms contained bacterial communities that were highly distinct from all other rooms, and spaces with high human occupant diversity and a high degree of connectedness to other spaces via ventilation or human movement contained a distinct set of bacterial taxa when compared to spaces with low occupant diversity and low connectedness. Within offices, the source of ventilation air had the greatest effect on bacterial community structure. CONCLUSIONS: Our study indicates that humans have a guiding impact on the microbial biodiversity in buildings, both indirectly through the effects of architectural design on microbial community structure, and more directly through the effects of human occupancy and use patterns on the microbes found in different spaces and space types. The impact of design decisions in structuring the indoor microbiome offers the possibility to use ecological knowledge to shape our buildings in a way that will select for an indoor microbiome that promotes our health and well-being.

Architectural design influences the diversity and structure of the built environment microbiome.

Buildings are complex ecosystems that house trillions of microorganisms interacting with each other, with humans and with their environment. Understanding the ecological and evolutionary processes that determine the diversity and composition of the built environment microbiome--the community of microorganisms that live indoors--is important for understanding the relationship between building design, biodiversity and human health. In this study, we used high-throughput sequencing of the bacterial 16S rRNA gene to quantify relationships between building attributes and airborne bacterial communities at a health-care facility. We quantified airborne bacterial community structure and environmental conditions in patient rooms exposed to mechanical or window ventilation and in outdoor air. The phylogenetic diversity of airborne bacterial communities was lower indoors than outdoors, and mechanically ventilated rooms contained less diverse microbial communities than did window-ventilated rooms. Bacterial communities in indoor environments contained many taxa that are absent or rare outdoors, including taxa closely related to potential human pathogens. Building attributes, specifically the source of ventilation air, airflow rates, relative humidity and temperature, were correlated with the diversity and composition of indoor bacterial communities. The relative abundance of bacteria closely related to human pathogens was higher indoors than outdoors, and higher in rooms with lower airflow rates and lower relative humidity. The observed relationship between building design and airborne bacterial diversity suggests that we can manage indoor environments, altering through building design and operation the community of microbial species that potentially colonize the human microbiome during our time indoors.